Collapse of dispersal trait diversity across a long-term chronosequence reveals a strong negative impact of frugivore extinctions on forest resilience

1. Understanding how seed dispersal disruption may alter plant community
diversity and dynamics over a large temporal scale remains a challenge.
Here, we use a long-term chronosequence to compare changes in the richness
and composition of different dispersal trait assemblages in communities
established before and after human colonisation in the Mascarene
archipelago. 2. Our study was located on Réunion on the slopes of the
Piton de la Fournaise, one of the most active volcanoes worldwide. We
analysed 151 vegetation surveys on lava flows dated between 1401-AD and
1956-AD and in tropical rainforests established on older substrata. We
defined five classes of substratum age, according to the well-known
chronology of native frugivore defaunation: “old substrata” and [1401,
1665[ when frugivores were abundant and diverse before permanent human
settlement; [1665, 1800[ when large-bodied frugivore populations were
strongly reduced; [1800, 1900[ when large-bodied frugivores went extinct
and small-bodied frugivores were still abundant; [1900, 1956] decline in
the population of small-bodied frugivores. Based on dispersal traits, we
categorised 146 native woody species as anemochorous, small fleshy-fruited
or large fleshy-fruited, i.e. plant of which fruit could not theoretically
be dispersed by extant frugivores. 3. Changes in dispersal trait diversity
strongly correlated with the chronology of defaunation. Species-rich
communities settled before human colonisation were strongly dominated by
fleshy-fruited species. Large fleshy-fruited plants in the oldest
communities settled after human colonisation declined markedly and almost
disappeared after 1800. The richness of small fleshy-fruited plants
decreased less rapidly across the chronosequence, with medium levels on
[1665, 1800[ and [1800, 1900[ lava flows and low levels on [1900, 1956]
lava flows. Conversely, the richness of anemochorous plants remained
unchanged. Communities settled before human colonisation had a similar
composition. Fleshy-fruited assemblages showed strong species loss across
the chronosequence, while anemochorous assemblages showed strong species
turnover, which was probably due to lower dispersal limitation. 4.
Synthesis. Our results provide the first insights into the tremendous
impact that frugivore extinction has on plant colonisation dynamics over
300 years. The dramatic loss of fleshy-fruited plant diversity on
historical lava flows highlights the irreplaceable dispersal role played
by frugivores, especially large-bodied species. The conservation of
plant-animal mutualistic interactions is invaluable and refaunation
efforts need to be undertaken in areas where frugivores have been
extirpated.